Context-dependency in carnivore co- occurrence across a multiuse conservation landscape
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20457758, 2022, 8, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/ece3.9239 by Cochrane Portugal, Wiley Online Library on [09/01/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License Received: 11 February 2022 | Revised: 1 August 2022 | Accepted: 3 August 2022 DOI: 10.1002/ece3.9239 RESEARCH ARTICLE Context-dependency in carnivore co-occurrence across a multi- use conservation landscape Gonçalo Curveira-Santos1 | Laura Gigliotti2 | Chris Sutherland3 | Daniela Rato1 | Margarida Santos-Reis1 | Lourens H. Swanepoel4,5 1 Centre for Ecology, Evolution and Environmental Changes (cE3c), Faculdade Abstract de Ciências, Universidade de Lisboa, Carnivore intraguild dynamics depend on a complex interplay of environmental affini- Lisbon, Portugal 2 Department of Environmental Science, ties and interspecific interactions. Context-dependency is commonly expected with Policy, and Management, University of varying suites of interacting species and environmental conditions but seldom em- California Berkeley, Berkeley, CA, USA 3 pirically described. In South Africa, decentralized approaches to conservation and the Centre for Research into Ecological and Environmental Modelling, University of St resulting multi-tenure conservation landscapes have markedly altered the environ- Andrews, St Andrews, UK mental stage that shapes the structure of local carnivore assemblages. We explored 4 Department of Zoology, School of assemblage-wide patterns of carnivore spatial (residual occupancy probability) and Mathematical & Natural Sciences, University of Venda, Thohoyandou, South temporal (diel activity overlap) co-occurrence across three adjacent wildlife-oriented Africa 5 management contexts—a provincial protected area, a private ecotourism reserve, and African Institute for Conservation Ecology, Levubu, South Africa commercial game ranches. We found that carnivores were generally distributed in- dependently across space, but existing spatial dependencies were context-specific. Correspondence Gonçalo Curveira-Santos, Centre for Spatial overlap was most common in the protected area, where species occur at Ecology, Evolution and Environmental higher relative abundances, and in game ranches, where predator persecution pre- Changes (cE3c), Faculdade de Ciências, Universidade de Lisboa, Lisbon, Portugal. sumably narrows the scope for spatial asymmetries. In the private reserve, spatial Email: gcurveirasantos@gmail.com co-occurrence patterns were more heterogeneous but did not follow a dominance Funding information hierarchy associated with higher apex predator densities. Pair-specific variability sug- African Institute for Conservation gests that subordinate carnivores may alternate between pre-emptive behavioral Ecology; Fundação para a Ciência e a Tecnologia, Grant/Award Number: strategies and fine-scale co-occurrence with dominant competitors. Consistency in PD/BD/114037/2015 and UID/ species-pairs diel activity asynchrony suggested that temporal overlap patterns in our BIA/00329/2019; National Geographic Society, Grant/Award Number: EC- study areas mostly depend on species' endogenous clock rather than the local con- 314R-18; South African Agency for text. Collectively, our research highlights the complexity and context-dependency of Science and Technology Advancement, Grant/Award Number: 107099 and guild-level implications of current management and conservation paradigms; specifi- 115040; Wild Tomorrow Fund cally, the unheeded potential for interventions to influence the local network of carni- vore interactions with unknown population-level and cascading effects. KEYWORDS camera trap, conservation management, co-occupancy, interspecific interactions, temporal overlap TA X O N O M Y C L A S S I F I C AT I O N Applied ecology; Community ecology; Landscape planning; Spatial ecology; Zoology This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. © 2022 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd. Ecology and Evolution. 2022;12:e9239. www.ecolevol.org | 1 of 17 https://doi.org/10.1002/ece3.9239
| 20457758, 2022, 8, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/ece3.9239 by Cochrane Portugal, Wiley Online Library on [09/01/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License 2 of 17 CURVEIRA-SANTOS et al. 1 | I NTRO D U C TI O N effects by, for instance, reducing risk-free and undisturbed space, inducing nocturnality, providing reduced or surplus resources (e.g., How species' resource use affinities and interspecific interactions Curveira-Santos et al., 2017; Mills & Harris, 2020). Hence, anthro- act to structure animal communities is a central tenet of coexistence pogenic influence may artificially narrow or dilute spatiotemporal theory (Macarthur & Levins, 1967; Schoener, 1974). Research on scopes for carnivore interactions, thus altering the landscape of co- spatial and temporal species' co-occurrence patterns (i.e., relative existence (Oriol-cotterill et al., 2015). Moreover, anthropic influence spatial and diel activity distributions) within mammalian carnivore on apex predators is particularly accentuated and well-described, guilds has assumed particular relevance (e.g., Davis et al., 2018). ranging from harmful interventions (e.g., direct persecution; Treves This is largely due to carnivores' propensity for agonistic interac- & Karanth, 2003) to directed conservation initiatives (Mossaz tions (Caro & Stoner, 2003; Donadio & Buskirk, 2006; Ritchie & et al., 2015; Sergio et al., 2008), influencing these species' ability Johnson, 2009) and their influence over ecosystem processes and to regulate guild and ecosystem dynamics (Dorresteijn et al., 2015; functioning (Estes et al., 2011; Prugh et al., 2009; Ripple et al., 2014). Haswell et al., 2015; Kuijper et al., 2016). Carnivore communities of Importantly, ongoing global declines of apex predators and shifts to- similar composition may thus exhibit fundamentally different spatio- ward mesopredator-dominated systems (Hoeks et al., 2020) have temporal structures across ecological contexts and, subsequently, motivated increasing calls for a more comprehensive understanding varying interaction dynamics. of predator community structure and its inclusion in conservation South Africa's diverse carnivore assemblages and the complexity and restoration plans (Jachowski et al., 2020; Ritchie et al., 2012; of the highly variable local conservation landscape are a pertinent Ritchie & Johnson, 2009; Svenning et al., 2016). model system to explore context-specific carnivore co-occurrence Fine-scale coexistence of sympatric carnivores species is me- patterns. Intraguild killing and interference exploitative competi- diated by a complex interplay of interspecific interactions beyond tion are pervasive among African carnivores (Caro & Stoner, 2003). individual resource preferences and species' fundamental niches Moreover, empirical evidence supports suppressive effects by the (Rosenzweig, 1966). Behavioral adjustments associated with inter- dominant apex predator, the African lion (Panthera leo), and other specific interactions include changes in space use and circadian ac- large carnivores, while the wide range of carnivore species' body tivity, to avoid confrontation with dominant species and/or partition sizes presupposes potential suppression-based cascades (Levi & the use of common resources (Karanth et al., 2017; Mills et al., 2019; Wilmers, 2012). Carnivore sympatry in South African landscapes is Monterroso et al., 2014, 2020; Robinson et al., 2014). Outcomes of thus expected to arise via a complex interplay of behavioral mech- antagonistic interactions may induce suppression-driven cascades anisms and co- occurrence patterns (Durant, 1998; Hayward & whereby apex predators limit large-bodied mesopredators, indirectly Slotow, 2009; Mills et al., 2019; Ramesh et al., 2017). benefiting smaller carnivores (Levi & Wilmers, 2012). Conversely, Notably, however, widespread human encroachment, wild- facilitative interactions, such as carrion provisioning by large car- life fencing (Packer et al., 2013), and decentralized approaches to nivore hunts, may promote carnivore co-occurrence and even en- conservation (Pitman et al., 2017) have markedly altered the stage hance suppression at the population level (Prugh & Sivy, 2020; Sivy upon which carnivore interactions take place. Private solutions to et al., 2017). When interspecific aggression and competition are not natural resource management have increasingly complemented the primary drivers, co-occurrence in space and time can result from the formal network of protected areas following changes in wild- trait similarities and common environmental and resource affinities life ownership rights, which prompted a large-scale land-use shift or stressors (i.e., habitat filtering; Rich et al., 2017). The interplay of from livestock farming to game ranching (ecotourism and/or hunt- co-occurrence patterns becomes particularly diffuse in species-rich ing; Pitman et al., 2017), giving rise to intricate multi-tenure con- carnivore assemblages, where heterogeneity in species' behavior, servation landscapes (Curveira-Santos, Sutherland, Santos-Reis, & morphology, and phylogeny influences the nature and strength of Swanepoel, 2021a; Di Minin et al., 2013). While large carnivores interspecific interactions at local scales. have been widely reintroduced into small and fenced reserves and A growing body of literature has helped elucidate the complexity often maintained at high densities (Mossaz et al., 2015), human pres- of carnivore community structure and intraguild interactions. Less at- ence and persecution of free-ranging species on game ranchland tention, however, has been given to underlying context-dependency, is common practice (Lindsey et al., 2008). Changes in guild com- which is generally assumed but often poorly described (Bar-Massada position are accompanied by varying levels of human disturbance & Belmaker, 2017; Chamberlain et al., 2014). Differences in commu- and its influence on resource availability across multiple land uses. nity composition and abundance of local carnivore species, as well as Together, these can deeply shape the structure of carnivore assem- diversity, availability, or spatial structuring of resources, can underly blages (Curveira-Santos, Sutherland, Tenan, et al., 2021b; Schuette context-specific carnivore spatiotemporal dependencies (Karanth et al., 2013) and potentially alter the underlying network of spe- et al., 2017). Human-caused disturbances are often the dominant cies interactions and community regulation pathways (Dorresteijn driver in forming ecological context, by modifying the landscapes et al., 2015). Nonetheless, context-dependent changes in carnivore and communities that predators interact with and within, albeit with assemblages have received little attention in carnivore-rich regions varying effects in direction and magnitude (reviewed in Sévêque of southern Africa, where context-dependency is likely to have pro- et al., 2020). Human influence often has broad and heterogeneous found effects.
| 20457758, 2022, 8, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/ece3.9239 by Cochrane Portugal, Wiley Online Library on [09/01/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License CURVEIRA-SANTOS et al. 3 of 17 Here, we link heterogeneity in carnivore co-occurrence patterns the production of wild ungulate species, and occasionally domestic to variation in conservation management models implemented in cattle, with large expanses of natural habitat and low human densi- South Africa. We evaluate spatial (residual occupancy correlation) ties. Leopards (Panthera pardus) and spotted hyenas (Crocuta Crocuta) and temporal (diel activity overlap) carnivore co-occurrence pat- are the only large carnivores that are observed in GR, where both terns across three adjacent wildlife-oriented management contexts, experience widespread persecution (Balme et al., 2010). The species spanning a 109- year- old provincial protected area (“conserva- composition of medium- (5–20 kg) and small-sized ( 0 . Within the indicator ( ) reserves hold a near-complete suite of large carnivores, although function, I(.), the variance of u ij is constrained by covariate effects African wild dogs (Lycaon pictus) only occasionally visit the PR. The and by a set of T latent variables lj = lj1 , … ,ljT and corresponding ( ) mosaic of commercial game ranches (GR) to the south is dedicated to species-specific latent variable coefficients i = i1 , … , iT . The ( )
| 20457758, 2022, 8, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/ece3.9239 by Cochrane Portugal, Wiley Online Library on [09/01/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License 4 of 17 CURVEIRA-SANTOS et al. F I G U R E 1 Camera-trapping surveys across three adjacent wildlife-oriented management contexts (provincial protected area, private ecotourism reserve, and commercial game ranches) in the Maputaland region of northern KwaZulu-Natal, South Africa latent variables are specified as random variables from a standard (TREE). We also considered site-level (camera) covariates influencing normal distribution and represent unmeasured site-level variation variation in detection probability; specifically, the average width of that is attributable to species spatial dependencies. The variance the trail structure targeted (TRAIL_W), and mean enhanced vegeta- of the residuals εij accounts for the variance absorbed by the la- tion index values (MODIS EVI datasets: https://lpdaac.usgs.gov/) for tent variables and is derived from adjusted variance σi2 values for the survey period as a proxy the vegetation density (VEG_D) in the each species i. For T latent variables and n species, the full species immediate vicinity (30 m) of each site. Prior to analysis, we standard- correlation matrix R is derived from the correlation in the latent ized all area-specific covariates to have a mean of 0 and standard variables as R = T + diag 21 , 22 , … , 2n . deviation of 1. ( ) We were interested in the residual correlation in the occupancy In order to parse out context-specific residual occupancy cor- probability that cannot be explained by the environmental covariates relation patterns, we fitted a single global JSDM for each target in the model, that is, after accounting for species-specific baseline area, with the following shared formulation: environmental preferences. Therefore, we modeled species-specific (i) Occupancy site occupancy probability as a function of covariates shown to in- ( ) Zij = I uij > 0 fluence species' occupancy patterns in this dataset (see Curveira- Santos, Sutherland, Santos-Reis, & Swanepoel, 2021a for details), uij = 0,i + 1,i TREEj + lj j + ij namely remote-sensed tree cover estimates within a 500 m radius buffer around each camera station (MODIS vegetation continuous T fields; DiMiceli et al., 2011) as a measure of the spectrum of vegeta- ∑ 2i = 1 − 2it tion structure ranging from open grasslands to woodland savannas t=1
| 20457758, 2022, 8, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/ece3.9239 by Cochrane Portugal, Wiley Online Library on [09/01/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License CURVEIRA-SANTOS et al. 5 of 17 ij ∼ Normal 0, 2i co-occurrence estimates as a function of the species-pair traits. ( ) For spatial co-occurrence patterns, we fit generalized linear mod- (ii) Detection els with the pairwise residual occupancy correlation as the response ( ) variable assuming Gaussian errors and an identity link to accommo- yij ∼ Binomial kj ,zij x pij date the [−1,1] distribution of this response variable. For temporal ( ) co-occurrence, we implemented beta regression models with the logit pi,j = 0,i + 1,i TRAIL _ Wj + 2,i VEG _ Dj temporal activity overlap coefficient as the response variable given the [0,1] distribution of these estimates (Douma & Weedon, 2019). The species-specific regression coefficients 1:2,i and 1:2,i (say ) For each response, we created an a priori global model based on are treated as species-specific random effects from a community- the additive effect of the dominance hierarchy within the carnivore level distribution: guild (i.e., proxy for top-down pressure) and pairwise measures of ecological similarity. To formally identify and describe how the na- ture and strength of each covariate effect varies across management ( ) i ∼ Normal , contexts, we modeled all covariate effects as interacting with the We fitted the JSDMs with 7, 6, and 5 latent variables for PA, PR, and three-level “area” covariate (i.e., PA, PR, and GR). GR, respectively, corresponding to about n/2 latent variables neces- Dominance hierarchy covariates included the different combi- sary to approximate the residual correlation matrix when there are nations of species' size-b ased hierarchy ranks (e.g., “Apex|Large,” n species in a community (Tobler et al., 2019). We implemented our and “Large|Medium”) coded as binary variables (Appendix B: models in the BUGS language using the JAGS software (Plummer, Table B1). Lions were ranked as the apex predator, non-apex spe- 2003) through R. For each co-occurrence model, we generated three cies >20 kg as large carnivores, species 5–20 kg as medium-sized MCMC chains with 30,000 iterations after a 10,000 iteration burn-in carnivores, and species 1 h after the last detection of the same spe- categories divided by the total number of unique food categories cies, converted to solar time to facilitate ecological interpretation. used by the pair; from Caro & Stoner, 2003), whether a pair in- To describe the general activity period of each species, we used cluded two species of the same hierarchy rank (proxy for lateral the function “modal.region.circular” to calculate the 95% activity competition), and whether a pair included species from the same isopleth. We used the function “getBandWidth” to calculate the family (phylogeny effect, proxy for relatedness). Additionally, we best smoothing parameter (κ) for each species and maintained the modeled the effect of the body-mass ratio of pairs (including a highest value when comparing activity patterns. Finally, using the quadratic relationship) to represent the suggested prevalence of function “totalvariation,” we calculated pairwise conditional activ- agonistic carnivore interactions at intermediate body-size differ- ity overlap coefficients as a measure of temporal co-o ccurrence; ences (body-mass ratios between 2 and 5.4) when the species ranging from 0, for perfect activity dissimilarity, to 1, for full inter- are similar enough in size to compete for same prey but different section of activity periods (95% isopleths). enough so that the larger size of the aggressor entails a low risk of injury (Donadio & Buskirk, 2006). This variable was highly cor- related with diet overlap (r = 0.70), and to prevent collinearity is- 2.4 | Drivers of co-occurrence sues (Dormann et al., 2013), we retained only the body-mass ratio in the global models since it led to an higher R 2 for both the spatial To investigate drivers of spatial and temporal co-occurrence and and temporal dimensions. Finally, we considered the effects of the how these vary across management contexts, we modeled our species spatial co-o ccurrence on temporal overlap and temporal
| 20457758, 2022, 8, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/ece3.9239 by Cochrane Portugal, Wiley Online Library on [09/01/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License 6 of 17 CURVEIRA-SANTOS et al. overlap on spatial co-o ccurrence to evaluate complementarity in co-occurrence between strictly nocturnal and diurnal species (0.00 niche partitioning patterns (Schoener, 1974). between slender [Herpestes sanguineus] and white-t ailed mongooses in both the PA and GR) to nearly complete activity overlap (0.97 be- tween leopard and serval [Leptailurus serval] in PA), thus indicating 3 | R E S U LT S an intricate temporal co-occurrence structure at the assemblage level (Figure 3b). Nonetheless, moderate- to- high overlap values Our dataset included a total of 4895 independent records of our (>0.5) were common in all three areas (69% in PA, 65% in PR, and 13 target wild carnivore species over 19,739 effective trap-days 57% in GR) due to a high number of predominantly nocturnal species (Appendix A: Table A2). We estimated spatial (residual correlation in all the assemblages. While the distribution of activity overlap val- in occupancy probability) and temporal (diel activity overlap) co- ues was similar between the protected area and the private reserve, occurrence for a total of 161 species pairs: 78 in PA, 55 in PR, and the pattern in the game ranches was bimodal, that is, either low or 28 in GR (Figure 2). high overlap. This was mostly attributable to the absence of several species with cathemeral activity patterns (e.g., lion and serval) rather than accentuated species-specific changes in activity (see below). 3.1 | Spatial co-occurrence The mean residual correlation in occupancy across all species 3.3 | Context-dependency in co-occurrence pair and area combinations was 0.06 ± 0.15 (mean ± SD), indicat- patterns ing that, at the assemblage level, there was neutral or independ- ent spatial co-o ccurrence. Area-specific means exhibited a similar Considering only species pairs present in more than one area pattern (PA = 0.06 ± 0.12, PR = 0.03 ± 0.16, and GR = 0.08 ± 0.11), (n = 55), context-dependency in pairwise spatial dependencies was albeit with large variation across species pairs (Figure 3a). Pairwise frequent whereas temporal co- occurrence patterns were largely residual occupancy correlation values ranged from 0.46 (95% consistent across areas (Figures 2 and 4; Appendix C: Figures C1 and Bayesian credible intervals, 0.27–0 .64), between the spotted hy- C2). Although weak residual occupancy correlation strength was the aena and the white-t ailed mongoose (Ichneumia albicauda) in the norm, nearly half (55%) of species pairs exhibited contrasting sig- private reserve, to −0.36 (−0.52 to −0.05), between the lion and nals in residual occupancy correlations across areas, that is, context- the large-spotted genet (Genetta maculata) also in the private re- dependency. Species with high probability of spatial avoidance in serve (Figure 2a; Appendix C: Figure C1). Positive spatial depend- one context (e.g., lion and large-spotted genet in PA), specifically, encies were predominant in both the protected area (67%) and the rarely did so in the others. Consistency in positive spatial dependen- game ranches (68%), while positive and negative residual correla- cies across contexts was more common; however, seldom pairs ex- tion values were more evenly distributed in the private reserve hibited correlation values that strongly departed from a hypothesis (56% vs. 44%, respectively, Figure 3a). However, strong evidence of independence (>0.9 probability) in different contexts. Conversely, for non-independent spatial co-o ccurrence patterns (>0.9 prob- species' temporal co-occurrence patterns were similar between con- ability of a different than zero correlation) was only observed in 14 texts, with 75% of pair-specific diel activity overlap differences of out of 161 pair-by-area combinations; 12 of which were positive ≤0.1 across areas. (five in PA, five in PR, and three in GR) and only two were negative (one in PA and PR each). Notably, the strength of negative spa- tial co-o ccurrence signals in game ranches was very low (>−0.1), 3.4 | Drivers of co-occurrence with no pairs exhibiting a >0.7 probability of a spatial avoidance pattern. The main drivers of carnivore spatial co- occurrence differed among management contexts (Table 1a). In the protected area, “Apex|Small” dominance hierarchy pairs, that is, pairs with the lion 3.2 | Temporal co-occurrence and a small-sized carnivore, exhibited lower spatial co-occurrence relative to all other pairs. In the private reserve, spatial co- Pairwise temporal activity overlap coefficients spanned a wide occurrence was lower for pairs from the same taxonomic family, range of values (Figure 2b; Appendix C: Figure C2), from no temporal but increased for pairs with higher diel activity overlap (i.e., pairs F I G U R E 2 Schematic depictions of pairwise (a) spatial and (b) temporal co-occurrence estimates within South African carnivore assemblages, across three adjacent management contexts (PA—provincial protected area; PR—private game reserve; GR—commercial game ranches). Body size in the carnivore assemblage decreases clockwise. Spatial co-occurrence patterns were estimated as pairwise residual occupancy correlation values from a hierarchical Bayesian joint species distribution model, and temporal co-occurrence expressed as pairwise coefficients of diel activity overlap from non-parametric, circular kernel density functions (see Methods). Line widths are proportional to the estimated co-occurrence values.
| 20457758, 2022, 8, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/ece3.9239 by Cochrane Portugal, Wiley Online Library on [09/01/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License CURVEIRA-SANTOS et al. 7 of 17 (a) (b) with high temporal overlap also exhibited high spatial overlap) and of the pairs' body-mass ratio. No clear associations were found to of intermediate body-mass differences (ratios ~2), that is, the re- explain variability in species' spatial co-occurrence in the game sidual occupancy correlation varied by a concave quadratic effect ranches.
| 20457758, 2022, 8, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/ece3.9239 by Cochrane Portugal, Wiley Online Library on [09/01/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License 8 of 17 CURVEIRA-SANTOS et al. (a) (b) F I G U R E 3 Assemblage-level (a) spatial (residual occupancy correlation) and (b) temporal (diel activity overlap) carnivore co-occurrence patterns in each of the three management contexts (PA—provincial protected area; PR—private game reserve; GR—commercial game ranches). Vertical lines mark area-specific medians (solid line) and 33 and 66% quantiles (dashed lines). The global model for the drivers of carnivore temporal co- 4 | DISCUSSION occurrence (Table 1b) indicated that, in all areas, pairings that in- cluded two small-sized species exhibited less temporal overlap than Our study provides important insights into context-dependency of other size pairings. Additionally, only in the private reserve, spe- carnivore spatial and temporal co-occurrence across a South African cies with high spatial overlap also exhibited high temporal activity multi- tenure conservation landscape. We found that carnivores overlap. generally distribute independently across space. Clear pairwise
| 20457758, 2022, 8, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/ece3.9239 by Cochrane Portugal, Wiley Online Library on [09/01/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License CURVEIRA-SANTOS et al. 9 of 17 (a) (b) F I G U R E 4 Context-dependency in (a) spatial (residual occupancy correlation) and (b) temporal (diel activity overlap) co-occurrence patterns for species pairs present in two or more areas (n = 55). PA, provincial protected area; PR, private game reserve; GR, commercial game ranches. For the spatial dimension, points in the top-right and bottom-left quadrants indicate a consistent co-occurrence signal, while top-left and bottom-right quadrants indicate context-dependent spatial dependencies. The color and shape of the points represents the proportion of the posterior distribution of the residual occupancy estimate with the same sign as the mean, that is, the probability for a different than zero correlation. For the temporal dimension, consistency in diel activity overlapped is expressed by proximity to the diagonal bar. Credible and confidence intervals were omitted for visual clarity. TA B L E 1 Beta coefficient estimates (±SE) for species-pair-specific covariates representing the hypothesized drivers of carnivore (a) spatial and (b) temporal co-occurrence (a) Spatial co-occurrence (b) Temporal co-occurrence Covariate PA PR GR PA PR GR Dominance hierarchy Apex|Small −0.18 ± 0.08 0.13 ± 0.08 - - - - Large|Medium - - - 0.58 ± 0.34 0.54 ± 0.46 0.98 ± 0.57 Same rank Large −0.07 ± 0.06 0.14 ± 0.09 0.21 ± 0.16 0.17 ± 0.46 0.20 ± 0.65 −0.91 ± 1.23 Medium −0.09 ± 0.10 −0.08 ± 0.16 0.02 ± 0.17 0.43 ± 0.74 1.23 ± 1.14 0.13 ± 1.27 Small −0.02 ± 0.06 0.12 ± 0.07 −0.02 ± 0.11 −1.73 ± 0.42 −1.15 ± 0.50 −1.98 ± 0.75 Same family 0.07 ± 0.04 −0.18 ± 0.06 −0.02 ± 0.11 0.46 ± 0.33 0.30 ± 0.47 −0.27 ± 0.84 Body-mass ratio −0.10 ± 0.05 0.14 ± 0.06 0.03 ± 0.10 −0.15 ± 0.37 0.11 ± 0.45 −0.78 ± 0.71 Body-mass ratio2 0.02 ± 0.01 −0.03 ± 0.01 −0.01 ± 0.02 −0.01 ± 0.06 −0.04 ± 0.07 0.07 ± 0.13 Temporal co-occurrence −0.08 ± 0.06 0.22 ± 0.08 0.06 ± 0.09 - - - Spatial co-occurrence - - - −1.04 ± 0.89 2.10 ± 0.84 1.70 ± 1.71 Global model R 2 0.25 0.39 Note: Well-supported coefficients (p < .05) are bolded. Abbreviations: PA, provincial protected area; PR, private game reserve; GR, commercial game ranches.
| 20457758, 2022, 8, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/ece3.9239 by Cochrane Portugal, Wiley Online Library on [09/01/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License 10 of 17 CURVEIRA-SANTOS et al. spatial dependencies were rare in all areas and seldom consistent Despite the predominance of independent or overlapping spatial across management and conservation models. Yet, as hypothesized, patterns, previous studies have suggested that, albeit rare, spatial a higher overall degree of spatial overlap was observed in the pro- avoidance is most common for pairs including large- bodied car- tected area, where species generally occur at higher relative abun- nivores (Davis et al., 2018), able to exert strong suppression over dances, and in game ranches, where human disturbance presumably subordinate species and induce avoidance behaviors (Donadio & narrows the scope for spatial asymmetries. In the private reserve, Buskirk, 2006; Ritchie & Johnson, 2009). We were particularly inter- spatial co-occurrence patterns were more heterogeneous but did ested in how the spatial structuring of the competitive environment not support the hypothesis of a well-marked dominance hierarchy may uphold coexistence between competition- depressed meso- associated with higher apex predator densities. In contrast, species- predators and the densely distributed apex predator population in pairs diel activity overlap was widespread and stable across areas, the private reserve. The few depressed residual occupancy correla- suggesting that, in our study areas, temporal asynchrony is less af- tion values observed included variable body-size pairings and domi- fected by the local context but regulated by each species' endoge- nance hierarchies. However, particularly in the protected area, small nous clock and adaptations to long-term coexistence with dominant carnivore species tended to spatially avoid lions. This is in line the predators. Our results suggest that carnivore interspecific interac- with recently uncovered susceptibility of small African carnivores tions may have limited expression in species co-occurrence patterns, to lion suppression (Curveira-Santos et al., 2022; Curveira-Santos, but existing spatial dependencies may reflect varying outcomes of Sutherland, Tenan, et al., 2021b). Unlike larger subordinate species, context-specific interactions. better equipped to escape and mitigate dangerous encounters while Irrespective of the context, the tendency for weak residual co-occurring with the apex predator, for small carnivores spatial spatial dependencies among species pairs indicates that carni- avoidance of lions may be a better strategy (Wirsing et al., 2010). vores were generally distributed independently over the landscape. Collectively, however, our results reinforce the notion that infor- But note that partitioning data by area for insights on context- mation on species spatial co-occurrence, while useful to character- dependency likely promotes the underestimation of co-occurrence ize the setting of potential ecological interactions, may be a poor strength (Tobler et al., 2019). Among observable spatial dependen- proxy for the actual signal and strength of interactions (Blanchet cies, we found that carnivore species were more likely to overlap et al., 2020). Detailed behavioral investigations and, importantly, spatially rather than avoid each other. Such observations corrobo- an increased understanding of carnivore interactions on population rate global-scale patterns of carnivore co-occurrence described by demography remain central to unraveling potential suppression pat- Davis et al. (2018) and the general assertion that the relative distri- terns (Miller et al., 2018). bution of sympatric carnivore species is mostly driven by species- Temporal partitioning is acknowledged as an important struc- specific preferences and resource use affinities. Other studies have turing force in carnivore assemblages, facilitating species coexis- found that sympatric carnivores with similar ecological traits pre- tence (Di Bitetti et al., 2010; Hayward & Slotow, 2009), particularly dominantly select for the same sites (Davis et al., 2018; Jonathan with increasing assemblage complexity (Monterroso et al., 2014). In Davies et al., 2007; Monterroso et al., 2020). In our assessment of our multi-carnivore system, this was evidenced by the full range of spatial dependencies, we attempted to account for environmental pairwise activity overlap values observed. Diel activity asynchrony filtering using a broad proxy of habitat structure (i.e., tree cover). was well-marked between the diurnal species (slender and banded However, this likely fails to fully capture other, more fine-scale and [Mungos mungo] mongooses) and remaining carnivores with reduced resource-relevant habitat selection factors, such as prey availability, or partial daytime activity (most large- and medium-sized species), which may underly local scale intraguild sympatry and heterogene- especially sympatric smaller carnivores with predominant nocturnal ity of the competitive environment (Amarasekare, 2003). Moreover, habits (genet, white-tailed mongoose and stripped polecat). This under a common stressor, species may aggregate in spatial refugia corroborates the general understanding of these species' ecology (Farris et al., 2017; Sogbohossou et al., 2018). In the game ranches, (Hunter, 2018). Among larger species, varying degrees of diurnal where larger and putative problem species (hyaena and leopard) and crepuscular activity, coupled with frequent asynchronous activ- experience persecution (Balme et al., 2010; Pitman et al., 2017), ity peaks, often resulted in moderate overlap values. Staple prey of these carnivores overlapped spatially. In such areas, the influence of large African carnivores are available throughout the day in African human disturbance on these species may incur fitness costs through savanna ecosystems, and competition avoidance has been proposed increased competition in shared, low-risk sites (Sévêque et al., 2020). as the primary cause of temporal partitioning among these carnivore While the reduced level of spatial asymmetries seemingly contra- species (Hayward & Slotow, 2009). dicts the “competitive exclusion” and “limiting similarity” principles Remarkably, we found that temporal overlap remained similar (Macarthur & Levins, 1967), our coarse-scale analysis of spatial de- across contexts, despite changes in guild composition, species rel- pendencies precluded exploration of fine-scale and spatiotempo- ative abundance, and other extrinsic factors. Previous studies have rally explicit avoidance and resource partitioning mechanisms. Many suggested plasticity in circadian activity patterns of carnivores may subordinate carnivores minimize the risk of encountering dominant enable coexistence across different ecological contexts (Monterroso competitors in resource-rich sites by fine-scale avoidance behaviors et al., 2014). However, our results suggest that, in our study areas, and constrained predation strategies (Ramesh et al., 2017). interspecific temporal partitioning among carnivores may be
| 20457758, 2022, 8, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/ece3.9239 by Cochrane Portugal, Wiley Online Library on [09/01/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License CURVEIRA-SANTOS et al. 11 of 17 maintained within species' own endogenous boundaries, which have spatial segregation more frequent in the private reserve. Compared evolved under long-term coexistence with dominant sympatric pred- with the private reserve, the scope for pre-emptive spatial avoid- ators. Importantly, low human encroachment in all our focal areas ance may be reduced because of widespread distribution of dom- likely does not translate into enough pressure to induce increased inant species in the protected area or limited low-risk spaces in nocturnality, as observed in other systems (Gaynor et al., 2018). It the game ranches. Detailed behavioral and demographic research is possible, however, that our area-level measure of activity overlap is needed to ascertain whether potentially increased carnivore en- fails to capture micro-adjustments in activity peaks across contexts. counter rates may enhance competitive and suppression pathways Interspecific interactions are multidimensional. Niche parti- or if spatial avoidance in the private reserve is itself the outcome of tioning theory suggests that in order to reduce competitive stress amplified competitive stress. Nevertheless, our results suggest that and facilitate coexistence, species converging along one niche understanding nonstationary properties of carnivore interactions axis, here space or time, segregate in complementary dimensions may be important to avoid erroneous extrapolation to local policies (Schoener, 1974). However, in both the protected area and game and practices (Rollinson et al., 2021). ranches, we found that species dependencies across the two studied With our study, we provide novel insights into the potential dimensions were largely unrelated. Notably, in the private reserve, of alternative management and conservation models to influence co-occurrence in space and time was the main underlying assem- community-wide ecological patterns and processes, specifically, the blage structure. Again, if environmental and resource affinities, and context-dependency of spatial and temporal associations of African not intraguild interactions and competition, are the primary driver of carnivore species. Our empirical exploration of co-occurrence pat- carnivore co-occurrence, such patterns may simply translate to com- terns emphasizes three important aspects underlying carnivore mon strategies by which groups of sympatric carnivores exploit their community research: the value of multispecies assessments (Heim environment in each context. Such reasoning reinforces the need to et al., 2019), the importance of predator behavior and interspe- consider the potential role of fine-scale behavioral adjustments for cific interactions (Ritchie & Johnson, 2009), and the prevalence a sound understanding of the mechanisms regulating co-occurrence of context- dependency in ecological interactions (Chamberlain patterns (Cusack et al., 2016; Vanak et al., 2013). Importantly, such et al., 2014). Understanding such aspects and how they relate to spatial and temporal relationships are theoretically underpinned by management interventions, particularly under southern Africa's the degree of trophic niche sharing (the third and missing fundamen- decentralized conservation approaches and predator-oriented man- tal niche axis, Schoener, 1974) and varying prey preferences and agement paradigms (Caro, 2015; Pitman et al., 2017), is of interest predatory strategies (Hayward & Kerley, 2008). to carnivore conservation efforts and for managing and protecting Prevalent patterns of independency in species spatial distri- food webs (Estes et al., 2011; Ritchie et al., 2012). However, our re- bution and consistent temporal activity overlap across areas did search also exemplifies the challenge of studying multiple species not fully support the hypothesized relationship between the local and environmental contexts, when resulting patterns are the likely management context and assemblage-level signals in species co- outcome of a complex web of spatially structured intraguild rela- occurrence. However, we observed that well-marked pairwise spa- tionships that may mask individual-species associations, themselves tial dependencies were idiosyncratic, with same species occurring ruled by inconspicuous idiocracies of species behavior. independently or with opposing signal in one of the adjacent land- scapes. Accordingly, the role of carnivore dominance relationships AU T H O R C O N T R I B U T I O N S and ecological similarity in mediating co-occurrence patterns was Gonçalo Curveira-Santos involved in conceptualization (lead); data context-specific. Such pair-by-area variability suggests that subor- curation (lead); formal analysis (lead); funding acquisition (support- dinate carnivores may alternate between pre-emptive behavioral ing); investigation (lead); methodology (lead); project administra- strategies to avoid dominant competitors and instances of fine-scale tion (equal); visualization (lead); writing—original draft (lead); and co-occurrence (Karanth et al., 2017). The latter may or may not be writing—review and editing (lead). Laura Gigliotti: involved in concep- accompanied by strategies to mitigate competitive stress at shared tualization (supporting); formal analysis (supporting); investigation sites, such as increased vigilance or facultative character displace- (supporting); methodology (supporting); writing—original draft (sup- ment (e.g., prey switching; Pfennig et al., 2006). The resulting co- porting); and writing—review and editing (equal). Chris Sutherland occurrence pattern and, importantly, the fitness impacts of species involved in conceptualization (supporting); formal analysis (sup- co-occurrence in a given context, likely depends on the complex in- porting); investigation (supporting); methodology (supporting); su- terplay of density-and trait-mediated (e.g., phenotypic plasticity and pervision (equal); and writing—review and editing (equal). Daniela body-size asymmetry) effects and characteristics of the local envi- Rato involved in conceptualization (supporting); formal analysis ronment (e.g., landscape features, resource availability and diversity, (supporting); investigation (supporting); methodology (supporting); and disturbance; Werner & Peacor, 2003). review and editing (supporting). Margarida Santos- and writing— By closely inspecting changes in co-occurrence of species pairs Reis involved in conceptualization (supporting); funding acquisition with spatial dependencies of varying signal across areas, we ob- (supporting); methodology (supporting); supervision (equal); and served that spatial overlap between the same species was generally writing—review and editing (equal). Lourens H. Swanepoel involved more common in both the protected area and game ranches, and in conceptualization (supporting); data curation (supporting); formal
| 20457758, 2022, 8, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/ece3.9239 by Cochrane Portugal, Wiley Online Library on [09/01/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License 12 of 17 CURVEIRA-SANTOS et al. analysis (supporting); funding acquisition (lead); investigation (sup- Curveira-Santos, G., Sutherland, C., Tenan, S., Fernández-Chacón, porting); methodology (supporting); project administration (lead); A., Mann, G. K. H., Pitman, R. T., & Swanepoel, L. H. (2021b). Mesocarnivore community structuring in the presence of Africa's supervision (equal); and writing—review and editing (equal). apex predator. Proceedings of the Royal Society B: Biological Sciences, 288, 20202379. AC K N OW L E D G M E N T S Curveira-Santos, G., Gigliotti, L., Silva, A. P., Sutherland, C., Foord, S., We thank the iSimangaliso Authority, Ezemvelo KZN Wildlife, the Santos-Reis, M., & Swanepoel, L. H. (2022). Broad aggressive inter- actions among African carnivores suggest intraguild killing is driven Mun- ya- wana Conservancy, reserves' staff, and ranch- owners by more than competition. Ecology, 103, 1–12. for supporting this research. We also thank everyone who as- Cusack, J. J., Dickman, A. J., Kalyahe, M., Rowcliffe, J. M., Carbon, C., sisted with fieldwork. This research was funded by South Africa's Macdonald, D. W., & Coulson, T. (2016). Revealing kleptoparasitic National Research Foundation (UID: 107099 and 115040), African and predatory tendencies in an African mammal community using camera traps: a comparison of spatiotemporal approaches. Oikos, Institute for Conservation Ecology, National Geographic Society 125, 336–3 42. (EC-314R-18) and Wild Tomorrow Fund. G.C.-S. and M.S.-R . were Davis, C. L., Rich, L. N., Farris, Z. J., Kelly, M. J., Di Bitetti, M. S., Di funded by Fundacão para a Ciência e a Tecnologia in the frame of Blanco, Y., Albanesi, S., Farhadinia, M. S., Gholikhani, N., Hamel, a doctoral grant (PD/BD/114037/2015) and the research unit (UID/ S., Harmsen, B. J., Wultsch, C., Kane, M. D., Martins, Q., Murphy, A. J., Steenweg, R., Sunarto, S., Taktehrani, A., Thapa, K., … Miller, BIA/00329/2019), respectively. D. A. W. (2018). Ecological correlates of the spatial co-occurrence of sympatric mammalian carnivores worldwide. Ecology Letters, 21, C O N FL I C T O F I N T E R E S T 1401–1412. The authors have no competing interests or conflict of interest to Di Bitetti, M. S., De Angelo, C. D., Di Blanco, Y. E., & Paviolo, A. (2010). declare. Niche partitioning and species coexistence in a neotropical felid as- semblage. Acta Oecologica, 36, 403–412. DiMiceli, C. M., Carroll, M. L., Sohlberg, R. A., Huang, C., Hansen, M. DATA AVA I L A B I L I T Y S TAT E M E N T C., & Townshend, J. R. G. (2011). 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